APOE-sensitive cholinergic sprouting compensates for hippocampal dysfunctions due to reduced entorhinal input

Journal of Neuroscience

Volumn 36, Issue 40, 2016, Pages 10472-10486

  Bott, Jean Bastien ^a,b   Héraud, Céline ^a,b   Cosquer, Brigitte ^a,b   Herbeaux, Karine ^a,b   Aubert, Julien ^a,b   Sartori, Maxime ^a,b   Goutagny, Romain ^a,b   Mathis, Chantal ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Alzheimer s disease; APOE4; Cholinergic sprouting; Entorhinal cortex; Hippocampal disconnection; Spatial memory

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E4; SLC17A7 PROTEIN, MOUSE; SLC18A3 PROTEIN, MOUSE; VESICULAR ACETYLCHOLINE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BARNES MAZE TEST; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DENTATE GYRUS; ELECTROSTIMULATION; ENTORHINAL CORTEX; FEMALE; FIRING RATE; GENOTYPE; HIPPOCAMPUS; HYPERACTIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MILD COGNITIVE IMPAIRMENT; MOUSE; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; SPATIAL MEMORY; SPIKE WAVE; STEREOTACTIC PROCEDURE; ANIMAL; BRAIN CIRCULATION; CHOLINERGIC NERVE; COGNITIVE DEFECT; CYTOLOGY; GENETICS; HUMAN; MAZE TEST; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; TRANSGENIC MOUSE; VASCULARIZATION;

ANIMALS; APOLIPOPROTEIN E4; CEREBROVASCULAR CIRCULATION; CHOLINERGIC FIBERS; COGNITIVE DYSFUNCTION; DENTATE GYRUS; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; OPTOGENETICS; PARASYMPATHETIC NERVOUS SYSTEM; SPATIAL MEMORY; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 84990841399     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1174-16.2016     Document Type: Article

References (63)

1. Altmann A, Tian L, Henderson VW, Greicius MD; Alzheimer’s Disease Neuroimaging Initiative Investigators (2014) Sex modifies the APOErelated risk of developing Alzheimer’s disease. Ann Neurol 75: 563-573. CrossRef Medline
2. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, Bassett SS, Shelton AL, Gallagher M (2012) Reduction of hippocampal Hyperactivity Improve cognition in amnestic mild cognitive impairment. Neuron 74: 467-474. CrossRef Medline
3. Bakker A, Albert MS, Krauss G, Speck CL, GallagherM (2015) Response of the medial temporal lobe network in amnestic mild cognitive impairment to therapeutic intervention assessed by fMRI and memory task performance. Neuroimage Clin 7: 688-698. CrossRef Medline
4. Barabash A, Marcos A, Ancín I, Vázquez-Alvarez B, de Ugarte C, Gil P, Fernández C, Encinas M, Ló pez-Ibor JJ, Cabranes JA (2009) APOE, ACT and CHRNA7 genes in the conversion from amnestic mild cognitive impairment to Alzheimer’s disease. Neurobiol Aging 30: 1254-1264. CrossRef Medline
5. Blain JF, Sullivan PM, Poirier J (2006) A deficit in astroglial organization causes the impaired reactive sprouting in humain apolipoprotein E4 targeted replacement mice. Neurobiol Dis 21: 505-514. CrossRef Medline
6. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: A platform for analyzing neural signals. J Neurosci Methods 192: 146-151. CrossRef Medline
7. Bott JB, Cosquer B, Héraud C, Zerbinatti C, Kelche C, Cassel JC, Mathis C (2013) Reduced plasticity and mild cognitive impairment-like deficits after entorhinal lesions in hAPP/APOE4 mice. Neurobiol Aging 34: 2683-2693. CrossRef Medline
8. Bour A, Grootendorst J, Vogel E, Kelche C, Dodart JC, Bales K, Moreau PH, Sullivan PM, Mathis C (2008) Middle-aged human apoE4 targetedreplacement mice show retention deficits on a wide range of spatial memory tasks. Behav Brain Res 193: 174-182. CrossRef Medline
9. Bragin A, Jandó G,Nádasdy Z, van Landeghem M, BuzsákiG (1995) DentateEEG spikes and associated interneuronal population burts in the hippocampal hilar region of the rat. J Neurophysiol 73: 1691-1705. Medline
10. Croxson PL, Browning PG, Gaffan D, Baxter MG (2012) Acetylcholine facilitates recovery of episodic memory after brain damage. J Neurosci 32: 13787-13795. CrossRef Medline
11. DeKosky ST, Ikonomovic MD, Styren SD, Beckett L, Wisniewski S, Bennett DA, Cochran EJ, Kordower JH, Mufson EJ (2002) Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann Neurol 51: 145-155. CrossRef Medline
12. Dickerson BC, Sperling RA (2008) Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: Insights from functional MRI studies. Neuropsychologia 46: 1624-1635. CrossRef Medline
13. Farlow MR, Lahiri DK, Poirier J, Davignon J, Hui S (1996) Apolipoprotein E genotype and gender influence response to tacrine therapy. Ann N Y Acad Sci 802: 101-110. CrossRef Medline
14. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE- ε4 allele. Proc Natl Acad Sci U S A 106: 7209-7214. CrossRef Medline
15. Foster TC, Deadwyler SA (1992) Acetylcholine modulates averaged sensory evoked responses and perforant path evoked field potentials in the rat dentate gyrus. Brain Res 587: 95-101. CrossRef Medline
16. Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, EdwardsRH (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304: 1815-1819. CrossRef Medline
17. Garibotto V, Tettamanti M, Marcone A, Florea I, Panzacchi A, Moresco R, Virta JR, Rinne J, Cappa SF, Perani D (2013) Cholinergic activity correlates with reserve proxies in Alzheimer’s disease. Neurobiol Aging 34: 2694.e13-18. CrossRef Medline
18. Geddes JW, Monaghan DT, Cotman CW, Lott IT, Kim RC, Chui HC (1985) Plasticity of hippocampal circuitry in Alzheimer’s disease. Science 230: 1179-1181. CrossRef Medline
19. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106: 43-53. CrossRef Medline
20. Gó mez-Isla T, Price JL, McKeel DW Jr, Morris JC, Growdon JH, Hyman BT (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer’s disease. J Neurosci 16: 4491-4500. Medline
21. Harrison FE, Reiserer RS, Tomarken AJ, McDonald MP (2006) Spatial and nonspatial escape strategies in the Barnes maze. Learn Mem 13: 809-819. CrossRef Medline
22. Henderson VW, Watt L, Buckwalter JG (1996) Cognitive skills associated with estrogen replacement in women with Alzheimer’s disease. Psychoneuroendocrinology 21: 421-430. CrossRef Medline
23. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL (1984) Alzheimer’s disease: Cell-specific pathology isolates the hippocampal formation. Science 225: 1168-1170. CrossRef Medline
24. Hyman BT, Van Hoesen GW, Kromer LJ, Damasio AR (1986) Perforant pathway changes and the memory impairment of Alzheimer’s disease. Ann Neurol 20: 472-481. CrossRef Medline
25. Jinde S, Zsiros V, Jiang Z, Nakao K, Pickel J, Kohno K, Belforte JE, Nakazawa K (2012) Hilar mossy cell degeneration causes transient dentate granule cell hyperexcitability and impaired pattern separation. Neuron 76: 1189-1200. CrossRef Medline
26. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421: 844-848. CrossRef Medline
27. Koepsell TD, Monsell SE (2012) Reversion from mild cognitive impairment to normal or near-normal cognition: Risk factors and prognosis. Neurology 79: 1591-1598. CrossRef Medline
28. Kordower JH, Chu Y, Stebbins GT, DeKosky ST, Cochran EJ, Bennett D, Mufson EJ (2001) Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Ann Neurol 49: 202-213. Medline
29. Laczó J, Andel R, Vlček K, Macoška V, Vyhnálek M, Tolar M, Bojar M, Hort J (2011) Spatial navigation and APOE in amnestic mild cognitive impairment. Neurodegener Dis 8: 169-177. CrossRef Medline
30. Loesche J, Steward O (1977) Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions. Brain Res Bull 2: 31-39. CrossRef Medline
31. Lynch G, Matthews DA, Mosko S, Parks T, Cotman C (1972) Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res 42: 311-318. CrossRef Medline
32. Mufson EJ, Binder L, Counts SE, DeKosky ST, de Toledo-Morrell L, Ginsberg SD, Ikonomovic MD, Perez SE, Scheff SW (2012) Mild cognitive impairment: Pathology and mechanisms. Acta Neuropathol 123: 13-30. CrossRef Medline
33. Neunuebel JP, Knierim JJ (2014) CA3 retrieves coherent representations from degraded input: Direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 81: 416-427. CrossRef Medline
34. Newhouse P, Dumas J (2015) Estrogen-cholinergic interactions: Implications for cognitive aging. Horm Behav 74: 173-185. CrossRef Medline
35. O’Leary TP, Brown RE (2012) The effects of apparatus design and test procedure on learning and memory performance of C57BL6J mice on Barnes maze. J Neurosci Methods 203: 315-324. CrossRef Medline
36. Pagliardini S, Gosgnach S, Dickson CT (2013) Spontaneous sleep-like brain state alternations and breathing characteristics in urethane anesthetized mice. PLoS One 8: E70411. CrossRef Medline
37. Palop JJ, Mucke L (2010) Amyloid-β-induced neuronal dysfunction in Alzheimer’s disease: From synapses toward neural networks. Nat Neurosci 13: 812-818. CrossRef Medline
38. Paré D, Llinás R (1995) Intracellular study of direct entorhinal inputs to field CA1 in the isolated guinea pig brain in vitro. Hippocampus 5: 115-119. CrossRef Medline
39. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, Ritchie K, Rossor M, Thal L, Winblad B (2001) Current concepts in mild cognitive impairment. Arch Neurol 58: 1985-1992. CrossRef Medline
40. Pfrieger FW (2010) Role of glial cells in the formation and maintenance of synapses. Brain Res Rev 63(1-2): 39-46.
41. Phinney AL, Calhoun ME, Woods AG, Deller T, Jucker M (2004) Stereological analysis of the reorganization of the dentate gyrus following entorhinal cortex lesion in mice. Eur J Neurosci 19: 1731-1740. CrossRef Medline
42. Poirier J (1999) Apolipoprotein E4, cholinergic integrity and the pharmacogenetics of alzheimer’s disease. J Psychiatry Neurosci 24: 147-153. Medline
43. Poirier J, Baccichet A, Dea D, Gauthier S (1993) Cholesterol synthesis and lipoprotein reuptake during synaptic remodeling in hippocampus in adult rats. Neuroscience 55: 81-90. CrossRef Medline
44. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, Mahley RW, Mucke L (1998) Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: Increased susceptibility of females. Proc Natl Acad Sci U S A 95: 10914-10919. CrossRef Medline
45. Ray NJ, Metzler-Baddeley C, Khondoker MR, Grothe MJ, Teipel S, Wright P, Heinsen H, Jones DK, Aggleton JP, O’Sullivan MJ (2015) Cholinergic basal forebrain structure influences the reconfiguration of white matter connections to support residual memory in mild cognitive impairment. J Neurosci 35: 739-747. CrossRef Medline
46. Rolls ET (2013) The mechanisms for pattern completion and pattern separation in the hippocampus. Front Syst Neurosci 7: 74. CrossRef Medline
47. Roof RL, Zhang Q, Glasier MM, Stein DG (1993) Gender-specific impairment on Morris water maze task after entorhinal cortex lesion. Behav Brain Res 57: 47-51. CrossRef Medline
48. Roses AD (1996) Apolipoprotein E alleles as risk factors in Alzheimer’s disease. Annu Rev Med 47: 387-400. CrossRef Medline
49. Scheff SW, Price DA, Schmitt FA, Mufson EJ (2006) Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 27: 1372-1384. CrossRef Medline
50. Schneider LS, Farlow MR, Henderson VW, Pogoda JM (1996) Effects of estrogen replacement therapy on response to tacrine in patients with Alzheimer’s disease. Neurology 46: 1580-1584. CrossRef Medline
51. Selkoe DJ (2012) Preventing Alzheimer’s disease. Science 337: 1488-1492.CrossRef Medline
52. Stein DG (2001) Brain damage, sex hormones and recovery: A new role for progesterone and estrogen? Trends Neurosci 24: 386-391. CrossRef Medline
53. Steward O (1992) Signals that induce sprouting in the central nervous system: Sprouting is delayed in a strain of mouse exhibiting delayed axonal degeneration. Exp Neurol 118: 340-351. CrossRef Medline
54. Stone DJ, Rozovsky I, Morgan TE, Anderson CP, Finch CE (1998) Increased synaptic sprouting in response to estrogen via an apolipoprotein E-dependent mechanism: Implications for Alzheimer’s disease. J Neurosci 18: 3180-3185. Medline
55. Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ (1997) Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 56: 933-944. CrossRef Medline
56. Teles-Grilo Ruivo LM, Mellor JR (2013) Cholinergic modulation of hippocampal network function. Front Synaptic Neurosci 5: 2. CrossRef Medline
57. Toumane A, Durkin T, Marighetto A, Galey D, Jaffard R (1988) Differential hippocampal and cortical cholinergic activation during the acquisition, retention, reversal and extinciton of a spatial discrimination in an 8-arm radial maze by mice. Behav Brain Res 30: 225-234. CrossRef Medline
58. van Strien NM, Cappaert NL, Witter MP (2009) The anatomy of memory: An interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10: 272-282. CrossRef Medline
59. Vandecasteele M, Varga V, erényi A, Papp E, Barthó P, Venance L, Freund TF, Buzsáki G (2014) Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhance theta oscillations in the hippocampus. Proc Natl Acad SciU S A111: 13535-13540. CrossRef Medline
60. Wang L, Day J, Roe CM, Brier MR, Thomas JB, Benzinger TL, Morris JC, Ances BM (2014) The effect of APOE e4 allele on cholinesterase inhibitors in patients with Alzheimer disease. Alzheimer Dis Assoc Disord 28: 122-127. CrossRef Medline
61. Xu WL, Caracciolo B, Wang HX, Santoni G, Winblad B, Fratglioni L (2013) Accelerated progression from mild cognitive impairment to dementia among APOE ε4ε4 carriers. J Alzheimers Dis 33: 507-515. CrossRef Medline
62. Yassa MA, Stark SM, Bakker A, Albert MS, Gallagher M, Stark CE (2010) High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. Neuroimage 51: 1242-1252. CrossRef Medline
63. Yassa MA, Mattfeld AT, Stark SM, Stark CE (2011) Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proc Natl Acad Sci U S A 108: 8873-8878. CrossRef Medline